Biomechanics of the cervical spine. I Normal kinematics.pdf

Clinical Biomechanics 15 (2000) 633±648

www.elsevier.com/locate/clinbiomech

Review paper

Biomechanics of the cervical spine. I: Normal kinematics

Nikolai Bogduk a, * , Susan Mercer b

Newcastle Bone and Joint Institute, University of Newcastle, Royal Newcastle Hospital, Level 4, David Maddison Building, Newcastle, NSW 2300,

Australia

Department of Anatomy, University of Otago, Dunedin, New Zealand

Abstract

This review constitutes the ®rst of four reviews that systematically address contemporary knowledge about the mechanical

behavior of the cervical vertebrae and the soft-tissues of the cervical spine, under normal conditions and under conditions that result

in minor or major injuries. This ®rst review considers the normal kinematics of the cervical spine, which predicates the appreciation

of the biomechanics of cervical spine injury. It summarizes the cardinal anatomical features of the cervical spine that determine how

the cervical vertebrae and their joints behave. The results are collated of multiple studies that have measured the range of motion of

individual joints of the cervical spine. However, modern studies are highlighted that reveal that, even under normal conditions,

range of motion is not consistent either in time or according to the direction of motion. As well, detailed studies are summarized that

reveal the order of movement of individual vertebrae as the cervical spine ¯exes or extends. The review concludes with an account of

the location of instantaneous centres of rotation and their biological basis.

Relevance

The facts and precepts covered in this review underlie many observations that are critical to comprehending how the cervical

spine behaves under adverse conditions, and how it might be injured. Forthcoming reviews draw on this information to explain how

injuries might occur in situations where hitherto it was believed that no injury was possible, or that no evidence of injury could be

Keywords: Cervical spine; Biomechanics; Movements; Anatomy

1. Introduction

therefore, predicated by the anatomy of the bones that

make up the neck and the joints that they form.

Amongst its several functions, the head can be re-

garded as a platform that houses the sensory apparatus

for hearing, vision, smell, taste and related lingual and

labial sensations. In order to function optimally, these

sensory organs must be able to scan the environment

and be delivered towards objects of interest. It is the

cervical spine that subserves these facilities. The cervical

spine constitutes a device that supports the sensory

platform, and moves and orientates it in three-dimen-

sional space.

The movements of the head are executed by muscles

but the type of movements possible depend on the shape

and structure of the cervical vertebrae and interplay

between them. The kinematics of the cervical spine are,

2. Functional anatomy

For descriptive purposes, the cervical spine can be

divided and perceived as consisting of four units, each

with a unique morphology that determines its kine-

matics and its contribution to the functions of the

complete cervical spine. In anatomical terms the units

are the atlas, the axis, the C2±3 junction and the re-

maining, typical cervical vertebrae. In metaphorical,

functional terms these can be perceived as the cradle, the

axis, the root, and the column.

2.1. The cradle

Corresponding author.

E-mail address: mgillam@mail.newcastle.edu.au (N. Bogduk).

The atlas vertebra serves to cradle the occiput. Into

its superior articular sockets it receives the condyles of

the occiput. The union between the head and atlas,

PII: S 0 2 6 8 - 0 0 3 3 ( 0 0 ) 0 0 034-6

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N. Bogduk, S. Mercer / Clinical Biomechanics 15 (2000) 633±648

through the atlanto-occipital joints, is strong, and allows

only for nodding movements between the two struc-

tures. In all other respects the head and atlas move and

function essentially as one unit.

The stability of the atlanto-occipital joint stems

largely from the depth of the atlantial sockets. The side

walls of the sockets prevent the occiput from sliding

sideways; the front and back walls prevent anterior and

posterior gliding of the head, respectively. The only

physiological movements possible at this joint are ¯ex-

ion and extension, i.e. nodding. These are possible be-

cause the atlantial sockets are concave whereas the

occipital condyles are convex.

Flexion is achieved by the condyles rolling forwards

and sliding backwards across the anterior walls of their

sockets (Fig. 1). If the condyles only rolled, they would

roll up and over the anterior wall of their sockets. Axial

forces exerted by the mass of the head or the muscles

causing ¯exion prevent this upward displacement and

cause the condyles to slide downwards and backwards

across the concave surface of the socket. Thereby the

condyles remain within their sockets, and the composite

movement is a rotation, or a spin, of each condyle across

the surface of its socket. A converse combination of

movements occurs in extension. This combination of

roll and contrary glide is typical of condylar joints.

The ultimate restraint to ¯exion and extension of the

atlanto-occipital joint is impaction of the rim of the

socket against the base of the skull. Under normal

conditions, however, ¯exion is limited by tension in the

posterior neck muscles and by impaction of the sub-

mandibular tissues against the throat. Extension is lim-

ited by the occiput compressing the suboccipital

muscles.

Axial rotation and lateral ¯exion are not physiologi-

cal movements of the atlanto-occipital joints. They

cannot be produced in isolation by the action of mus-

cles. But they can be produced arti®cially by forcing the

head into these directions while ®xing the atlas. Axial

rotation is prohibited by impaction of the contralateral

condyle against the anterior wall of its socket and si-

multaneously by impaction of the ipsilateral condyle

Fig. 2. Right lateral views of axial rotation of the atlanto-occipital

joints. Rotation requires forward translation of one condyle and

backward translation of the other. Translation is possible only if the

condyles rise up the respective walls of the atlantial sockets. As a re-

sult, the occiput rises relative to its resting position (centre ®gure).

against the posterior wall of its socket. For the head to

rotate, the condyles must rise up their respective walls.

Consequently, the occiput must separate from the atlas

(Fig. 2). This separation is resisted by tension in the

capsules of the atlanto-occipital joints. As a result, the

range of motion possible is severely limited. Lateral

¯exion is limited by similar mechanisms. For lateral

¯exion to occur the contralateral condyle must lift out of

its socket, which engages tension in the joint capsule.

2.2. The axis

Carrying the head the atlas sits on the atlas, with the

weight being borne through the lateral atlanto-axial

joints. After weight-bearing, the cardinal function of the

atlanto-axial junction is to permit a large range of axial

rotation. This movement requires the anterior arch of

the atlas to pivot on the odontoid process and slide

around its ipsilateral aspect; this movement being

accommodated at the median atlanto-axial joint

(Fig. 3(A)). Meanwhile, at the lateral atlanto-axial joint

the ipsilateral lateral mass of the atlas must slide back-

wards and medially while the contralateral lateral mass

must slide forwards and medially (Fig. 3).

Radiographs of the lateral atlanto-axial joints belie

their structure. In radiographs the facets of the joint

appear ¯at, suggesting that during axial rotation the

lateral atlanto-axial joints glide across ¯at surface. But

radiographs do not reveal cartilage. The articular car-

tilages both of the atlantial and the axial facets of the

Fig. 1. Right lateral views of ¯exion and extension of the atlanto-oc-

cipital joints. The centre ®gure depicts the occipital condyle resting in

the atlantial socket in a neutral position. The dots are reference points.

In ¯exion the head rotates forwards but the condyle also translates

backwards, as indicated by the displacement of the references dot. A

converse combination of movements occurs in extension.

Fig. 3. Atlanto-axial rotation. A: top view. The anterior arch of the

atlas (shaded) glides around the odontoid process. B: right lateral view.

The lateral mass of the atlas subluxates forwards across the superior

articular process of the axis.

N. Bogduk, S. Mercer / Clinical Biomechanics 15 (2000) 633±648

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Fig. 4. Lateral view of a right lateral atlanto-axial joint (centre ®gure)

showing the biconcave structure of the articular cartilages. Upon

forward or backward displacement, the lateral mass of the atlas settles

as it slips down the slope of the cartilage.

Fig. 5. The mechanism of paradoxical movements of the atlas. In the

neutral position (centre ®gure) the atlas is balanced on the convexities of

its articular cartilages. If the atlas is compressed anterior to the balance

point, it ¯exes. If compressed behind the balance point, it extends.

joint are convex, rendering the joint biconvex [1] (Fig. 4).

The spaces formed anteriorly and posteriorly, where the

articular surfaces diverge, are ®lled by intra-articular

meniscoids [2]. In the neutral position the summit of the

atlantial convexity rests on the convexity of the axial

facet. As the atlas rotates, however, the ipsilateral at-

lantial facet slides down the posterior slope of its axial

fact, and the contralateral atlantial facet slides down the

anterior slope of its facet. As a result, during axial ro-

tation the atlas descends, or nestles into the axis (Fig. 4).

Upon reversing the rotation the atlas rises back onto the

summits of the facets.

Few muscles act directly on the atlas. The levator

scapulae arises from its transverse process but uses this

point of suspension to act on the scapulas; it does not

move the atlas. Obliquus superior and rectus capitis

posterior minor arise from the atlas and act on the oc-

ciput, as do rectus anterior and rectus lateralis. At-

taching to the anterior tubercle, longus cervicis is the

one muscle that acts directly on the atlas, to ¯ex it. But

paradoxically there is no antagonist to this muscle.

This paradox underscores the fact that the atlas acts

as a passive washer, interposed between the head and

the cervical spine proper. Its movements are essentially

passive and governed essentially by the muscles that act

on the head. Accordingly, rotation of the atlas is

brought about by splenius capitis and sternocleidomas-

toid acting on the head. Torque is then transferred from

the head, though the atlanto-occipital joints, to the at-

las. The ®bres of splenius cervics that insert into the

atlas supplement this eect.

The passive movements of the atlas are most evident

in ¯exion/extension of the neck where, indeed, the atlas

exhibits paradoxical motion. At full ¯exion of the neck

the atlas can extend, and usually does so [3]. This arises

because the atlas, sandwiched between the head and

axis, and balanced precariously on the summits of the

lateral atlanto-axial facets, is subject to compression

loads. If the net compression passes anterior to the

contact point in the lateral atlanto-axial joint, the lateral

mass of the atlas will be squeezed into ¯exion (Fig. 5).

Conversely, if the line of compression passes behind the

contact point, the atlas will extend; even if the rest of the

cervical spine ¯exes (Fig. 5). If, during ¯exion, the chin is

tucked backwards, paradoxical extension of the atlas is

virtually assured, because retraction of the chin favours

the line of weight-bearing of the skull to fall behind the

centre of the lateral atlanto-axial joints.

The restraints to ¯exion/extension of the atlas have

never been formally established. No ligaments are dis-

posed to limit this motion. The various atlanto-occipital

membranes are fascial in nature and would not consti-

tute substantive ligamentous restraints. Essentially, the

atlas is free to ¯ex or extend until the posterior arch hits

either the occiput or the neural arch of C2, respectively.

The restraints to axial rotation are the capsules of the

lateral atlanto-axial joints and the alar ligaments. The

capsules contribute to a minor degree; the crucial re-

straints are the alar ligaments [4]. Dislocation of the

atlas in rotation does not occur while so long as the alar

ligaments remain intact. This feature further under-

scores the passive nature of the atlas, for the alar liga-

ments do not attach to the atlas; rather, they bind the

head to the odontoid process of the axis. By limiting

the range of motion of the head they secondarily limit

the movement of the atlas.

Backward sliding of the atlas is limited absolutely by

impaction of the anterior arch of the atlas against the

odontoid process, but there is no bony obstruction to

forward sliding. That movement is limited by the

transverse ligament of the atlas and the alar ligaments.

As long as either ligament remains intact, dislocation of

the atlas is prevented [5].

Lateral gliding involves the ipsilateral lateral mass of

the atlas sliding down the slope of its supporting supe-

rior articular process while the contralateral lateral mass

slides upwards. The movement is primarily limited by

the contralateral alar ligament, but is ultimately blocked

by impaction of the lateral mass on the side of the

odontoid process [6].

2.3. The root

The C2±3 junction is commonly regarded as the

commencement of the typical cervical spine, where all

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N. Bogduk, S. Mercer / Clinical Biomechanics 15 (2000) 633±648

segments share the same morphological and kinematic

features. However, the C2±3 junction diers from other

segments in a subtle but obscure way.

The dierences in morphology are not readily ap-

parent and, for this reason, have largely escaped notice.

A pillar view of the region reveals the dierence. (A

pillar view is obtained by beaming X-rays upwards and

forwards through the cervical spine, essentially along the

planes of the zygapophysial joints.) In such a view

the body of the axis looks like a deep root, anchoring the

apparatus, that holds and moves the head, into the

typical cervical spine (Fig. 6). Moreover, in such view,

the atypical orientation of the C2±3 zygapophysial joints

is seen. Unlike the typical zygapophysial joints whose

planes are transverse, the superior articular processes of

C3 face not only upwards and backwards but also me-

dially, by about 40° [7]. Together, the processes of both

sides form a socket into which the inferior articular

processes of the axis are nestled. Furthermore, the su-

perior articular processes of C3 lie lower, with respect

to their vertebral body, than the processes of lower

segments [8].

These dierences in architecture imply that the C2±3

joints should operate in a manner dierent from that of

lower, typical cervical segments. One dierence is that

during axial rotation of the neck, the direction of cou-

pling with lateral ¯exion at C2±3 is opposite to that seen

at lower segments (see Table 4). Instead of bending to-

wards the same side as rotation, C2 rotates away from

that side, on the average. The lower location of the su-

perior articular process of C3 correlates with the lower

location of the axis of sagittal rotation of C2 (see

Fig. 14). Other dierences in how C2±3 operates have

not been elaborated, but the unique architecture of C2±3

suggests that further dierences are open to discovery.

2.4. The column

At typical cervical segments, the vertebral bodies are

stacked on one another, separated by intervertebral

discs. The opposing surfaces of the vertebral bodies,

however, are not ¯at as they are in the lumbar spine.

Rather, they are gently curved in the sagittal plane. The

anterior inferior border of each vertebral body forms a

lip that hangs downwards like a slight hook towards the

anterior superior edge of the vertebra below. Mean-

while, the superior surface of each vertebral body slopes

greatly downwards and forwards. As a result, the plane

of the intervertebral disc is set not perpendicular but

somewhat oblique to the long axes of the vertebral

bodies. This structure re¯ects, and is conducive to,

¯exion±extension being the cardinal movement of typi-

cal cervical segments.

The vertebral bodies are also curved from side-to-

side, but this curvature is not readily apparent. It is re-

vealed if sections are taken through the posterior ends of

the vertebral bodies, either parallel to the planes of the

zygapophysial joints, or perpendicular to these planes.

Such sections reveal that the inferior surface of the hind

end of the vertebral body is convex, and that convexity

is received by a concavity formed by the body below and

its uncinate processes (Fig. 7). The appearance is that of

an ellipsoid joint (like the wrist). This structure suggest

that vertebral bodies can rock side-to-side in the con-

cavity of the uncinate processes. Further consideration

reveals that this is so, but only in one plane.

If sections are taken through the cervical spine along

planes perpendicular to the zygapophysial joints, and if

the sections through the uncinate region and through

the zygapophysial joints are superimposed, the appear-

ance is revealing [9,10] (Fig. 8). The structure of the

interbody junction is ellipsoid and suggests that rocking

could occur between the vertebral bodies. However, in

this plane the facets of the zygapophysial joints are di-

rectly opposed. Therefore, any attempted rocking of the

vertebral body is immediately prevented by the facets

(Fig. 8).

If sections are taken through the plane of the zyga-

pophysial joints, the ellipsoid structure of the interbody

joint is again revealed, but the zygapophysial joints

Fig. 6. A tracing of a pillar view of the upper cervical spine, showing

the unique morphology of C2 (shaded). (A pillar view is a radiographic

projection of the cervical spline obtained by directing the beams up-

wards and forwards from behind the cervical spine, essentially along

the planes of the lower cervical zygapophysial joints.) Note how the

zygapophysial joints at lower levels (arrowed) are orientated trans-

versely whereas at C2±3 they are inclined medially, cradling the pos-

terior elements of the axis while its vertebral body dips like a deep root

into the cervical vertebral column.

N. Bogduk, S. Mercer / Clinical Biomechanics 15 (2000) 633±648

637

Fig. 9. The appearance, viewed from above, of superimposed sections

of a C5±6 cervical intervertebral joint taken through the uncinate

region and through the zygapophysial joints, along a plane parallel to

that of the zygapophysial joints. In this plane, if the C5 vertebral body

rotates, its inferior articular facets (iaf) are free to glide across the

surface of the superior articular facets of C6.

Fig. 7. A sketch of a section taken obliquely through the posterior end

of a C5±6 interbody joint, along a plane parallel to the plane of the

zygapophysial joints. Between the uncinate processes (u) the C6

vertebral body presents a concave articular surface that receives the

convex inferior surface of C5.

Fig. 8. The appearance, viewed from above, of a section of a C6±7

cervical intervertebral joint taken through the uncinate region and the

zygapophysial joints, along a plane perpendicular to the zygapophysial

joints. In this plane, if the C6 vertebral body rotates to the left, its right

inferior articular process (iap) immediately impacts, en face, into the

superior articular process (sap) of C7; which precludes lateral rotation

of C6.

present en face. Consequently the facets do not impede

rocking of the vertebral bodies in this plane. Indeed, the

facets slide freely upon one another (Fig. 9).

These observations indicate that the cervical inter-

vertebral joints are saddle joints: they consist of two

concavities facing one another and set at right angles to

one another [9,10]. Across the sagittal plane the inferior

surface of the vertebral body is concave downwards,

while across the plane of the zygapophysial joints the

uncinate region of the lower vertebral body is concave

Fig. 10. The saddle shape of cervical intervertebral joints. The inferior

surface of the upper vertebral body is concave downwards in the

sagittal plane (s). The superior surface of the lower vertebral body is

concave upwards in the transverse plane (t).

upwards (Fig. 10). This means that the vertebral body is

free to rock forwards in the sagittal plane, around a

transverse axis, and is free to rock side-to-side in the

place of the facets, around an axis perpendicular to the

facets (Fig. 11). Motion in the third plane ± side-to-side

around an oblique anterior ± posterior axis is precluded

by the orientation of the facets.

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